Cryo‐electron microscopy structure of the intact photosynthetic light‐harvesting antenna‐reaction center complex from a green sulfur bacterium

ABSTRACT The photosynthetic reaction center complex (RCC) of green sulfur bacteria (GSB) consists of the membrane‐imbedded RC core and the peripheric energy transmitting proteins called Fenna–Matthews–Olson (FMO). Functionally, FMO transfers the absorbed energy from a huge peripheral light‐harvestin...

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Veröffentlicht in:Journal of integrative plant biology 2023-01, Vol.65 (1), p.223-234
Hauptverfasser: Chen, Jing‐Hua, Wang, Weiwei, Wang, Chen, Kuang, Tingyun, Shen, Jian‐Ren, Zhang, Xing
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creator Chen, Jing‐Hua
Wang, Weiwei
Wang, Chen
Kuang, Tingyun
Shen, Jian‐Ren
Zhang, Xing
description ABSTRACT The photosynthetic reaction center complex (RCC) of green sulfur bacteria (GSB) consists of the membrane‐imbedded RC core and the peripheric energy transmitting proteins called Fenna–Matthews–Olson (FMO). Functionally, FMO transfers the absorbed energy from a huge peripheral light‐harvesting antenna named chlorosome to the RC core where charge separation occurs. In vivo, one RC was found to bind two FMOs, however, the intact structure of RCC as well as the energy transfer mechanism within RCC remain to be clarified. Here we report a structure of intact RCC which contains a RC core and two FMO trimers from a thermophilic green sulfur bacterium Chlorobaculum tepidum at 2.9 Å resolution by cryo‐electron microscopy. The second FMO trimer is attached at the cytoplasmic side asymmetrically relative to the first FMO trimer reported previously. We also observed two new subunits (PscE and PscF) and the N‐terminal transmembrane domain of a cytochrome‐containing subunit (PscC) in the structure. These two novel subunits possibly function to facilitate the binding of FMOs to RC core and to stabilize the whole complex. A new bacteriochlorophyll (numbered as 816) was identified at the interspace between PscF and PscA‐1, causing an asymmetrical energy transfer from the two FMO trimers to RC core. Based on the structure, we propose an energy transfer network within this photosynthetic apparatus. The structure of the intact photosynthetic complex of the green sulfur bacterium Chlorobaculum tepidum contains one reaction center, two asymmetrically binding Fenna‐Matthews‐Olson protein trimers, two novel subunits, and a new bacteriochlorophyll, providing insight into the energy transfer network within this photosynthetic apparatus.
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Functionally, FMO transfers the absorbed energy from a huge peripheral light‐harvesting antenna named chlorosome to the RC core where charge separation occurs. In vivo, one RC was found to bind two FMOs, however, the intact structure of RCC as well as the energy transfer mechanism within RCC remain to be clarified. Here we report a structure of intact RCC which contains a RC core and two FMO trimers from a thermophilic green sulfur bacterium Chlorobaculum tepidum at 2.9 Å resolution by cryo‐electron microscopy. The second FMO trimer is attached at the cytoplasmic side asymmetrically relative to the first FMO trimer reported previously. We also observed two new subunits (PscE and PscF) and the N‐terminal transmembrane domain of a cytochrome‐containing subunit (PscC) in the structure. These two novel subunits possibly function to facilitate the binding of FMOs to RC core and to stabilize the whole complex. A new bacteriochlorophyll (numbered as 816) was identified at the interspace between PscF and PscA‐1, causing an asymmetrical energy transfer from the two FMO trimers to RC core. Based on the structure, we propose an energy transfer network within this photosynthetic apparatus. The structure of the intact photosynthetic complex of the green sulfur bacterium Chlorobaculum tepidum contains one reaction center, two asymmetrically binding Fenna‐Matthews‐Olson protein trimers, two novel subunits, and a new bacteriochlorophyll, providing insight into the energy transfer network within this photosynthetic apparatus.</description><identifier>ISSN: 1672-9072</identifier><identifier>EISSN: 1744-7909</identifier><identifier>DOI: 10.1111/jipb.13367</identifier><identifier>PMID: 36125941</identifier><language>eng</language><publisher>China (Republic : 1949- ): Wiley Subscription Services, Inc</publisher><subject>Antennas ; Asymmetry ; Bacteria ; Bacterial Proteins - metabolism ; Bacteriochlorophyll ; Carcinoma, Renal Cell ; Chlorobi - chemistry ; Chlorobi - metabolism ; Cryoelectron Microscopy ; cryo‐electron microscopy ; Cytochrome ; Cytochromes ; Electron microscopy ; Energy transfer ; FMO protein ; Green sulfur bacteria ; green sulfur bacterium ; Kidney Neoplasms ; Microscopy ; Photosynthesis ; Photosynthetic apparatus ; Photosynthetic Reaction Center Complex Proteins - chemistry ; Photosynthetic Reaction Center Complex Proteins - metabolism ; reaction center ; Sulfur ; Sulfur bacteria ; Trimers</subject><ispartof>Journal of integrative plant biology, 2023-01, Vol.65 (1), p.223-234</ispartof><rights>2022 Institute of Botany, Chinese Academy of Sciences.</rights><rights>2023 Institute of Botany, Chinese Academy of Sciences</rights><rights>Copyright © Wanfang Data Co. 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Functionally, FMO transfers the absorbed energy from a huge peripheral light‐harvesting antenna named chlorosome to the RC core where charge separation occurs. In vivo, one RC was found to bind two FMOs, however, the intact structure of RCC as well as the energy transfer mechanism within RCC remain to be clarified. Here we report a structure of intact RCC which contains a RC core and two FMO trimers from a thermophilic green sulfur bacterium Chlorobaculum tepidum at 2.9 Å resolution by cryo‐electron microscopy. The second FMO trimer is attached at the cytoplasmic side asymmetrically relative to the first FMO trimer reported previously. We also observed two new subunits (PscE and PscF) and the N‐terminal transmembrane domain of a cytochrome‐containing subunit (PscC) in the structure. These two novel subunits possibly function to facilitate the binding of FMOs to RC core and to stabilize the whole complex. A new bacteriochlorophyll (numbered as 816) was identified at the interspace between PscF and PscA‐1, causing an asymmetrical energy transfer from the two FMO trimers to RC core. Based on the structure, we propose an energy transfer network within this photosynthetic apparatus. The structure of the intact photosynthetic complex of the green sulfur bacterium Chlorobaculum tepidum contains one reaction center, two asymmetrically binding Fenna‐Matthews‐Olson protein trimers, two novel subunits, and a new bacteriochlorophyll, providing insight into the energy transfer network within this photosynthetic apparatus.</description><subject>Antennas</subject><subject>Asymmetry</subject><subject>Bacteria</subject><subject>Bacterial Proteins - metabolism</subject><subject>Bacteriochlorophyll</subject><subject>Carcinoma, Renal Cell</subject><subject>Chlorobi - chemistry</subject><subject>Chlorobi - metabolism</subject><subject>Cryoelectron Microscopy</subject><subject>cryo‐electron microscopy</subject><subject>Cytochrome</subject><subject>Cytochromes</subject><subject>Electron microscopy</subject><subject>Energy transfer</subject><subject>FMO protein</subject><subject>Green sulfur bacteria</subject><subject>green sulfur bacterium</subject><subject>Kidney Neoplasms</subject><subject>Microscopy</subject><subject>Photosynthesis</subject><subject>Photosynthetic apparatus</subject><subject>Photosynthetic Reaction Center Complex Proteins - chemistry</subject><subject>Photosynthetic Reaction Center Complex Proteins - metabolism</subject><subject>reaction center</subject><subject>Sulfur</subject><subject>Sulfur bacteria</subject><subject>Trimers</subject><issn>1672-9072</issn><issn>1744-7909</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9kc9u1DAQhy0EomXhwgMgSwgJIaX438bJsawKFFWCQ--W1xnvepXYwXZow6mPwIEn5EnwsksPHPDF1ujzN5r5IfSckjNaztudG9dnlPNaPkCnVApRyZa0D8u7lqxqiWQn6ElKO0J4Q2r2GJ3wmrJlK-gp-rmKc_h19wN6MDkGjwdnYkgmjDNOOU4mTxFwsDhvATuftcl43IYc0uxLKTuDe7fZ5qLY6vgNUnZ-g7XP4L0uxQjlhyteA6UWsQnD2MMttjEMWONNBPA4Tb2dIl4XFKKbhqfokdV9gmfHe4Gu319crz5WV58_XK7OryrDGy4rygUXbWPJUtjOGGIbqqXuSAesI9CJtjPWgmCma8HUmku7bATVoC2xom74Ar06aG-0t9pv1C5M0ZeG6vvN7ZoRxgkldFm41wdujOHrVEZUg0sG-l57CFNSTNKatISKvfLlP-i9k0lJSv-mBLVAbw7UftUpglVjdIOOs6JE7SNV-0jVn0gL_OKonNYDdPfo3wwLQI9juB7m_6jUp8sv7w7S36HxsvE</recordid><startdate>202301</startdate><enddate>202301</enddate><creator>Chen, Jing‐Hua</creator><creator>Wang, Weiwei</creator><creator>Wang, Chen</creator><creator>Kuang, Tingyun</creator><creator>Shen, Jian‐Ren</creator><creator>Zhang, Xing</creator><general>Wiley Subscription Services, Inc</general><general>Research Institute for Interdisciplinary Science,and Graduate School of Natural Science and Technology,Okayama University,Okayama 700-8530,Japan%Department of Pathology of Sir Run Run Shaw Hospital,and Department of Biophysics,Zhejiang University School of Medicine,Hangzhou 310058,China</general><general>College of Life Science,Zhejiang University,Hangzhou 310058,China</general><general>Center of Cryo Electron Microscopy,Zhejiang University School of Medicine,Hangzhou 310058,China</general><general>Department of Pathology of Sir Run Run Shaw Hospital,and Department of Biophysics,Zhejiang University School of Medicine,Hangzhou 310058,China%College of Life Science,Zhejiang University,Hangzhou 310058,China%Department of Pathology of Sir Run Run Shaw Hospital,and Department of Biophysics,Zhejiang University School of Medicine,Hangzhou 310058,China%Key Laboratory of Photobiology,Institute of Botany,Photosynthesis Research Center,the Chinese Academy of Sciences,Beijing 100093,China%Key Laboratory of Photobiology,Institute of Botany,Photosynthesis Research Center,the Chinese Academy of Sciences,Beijing 100093,China</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QO</scope><scope>7T7</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>2B.</scope><scope>4A8</scope><scope>92I</scope><scope>93N</scope><scope>PSX</scope><scope>TCJ</scope></search><sort><creationdate>202301</creationdate><title>Cryo‐electron microscopy structure of the intact photosynthetic light‐harvesting antenna‐reaction center complex from a green sulfur bacterium</title><author>Chen, Jing‐Hua ; 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Functionally, FMO transfers the absorbed energy from a huge peripheral light‐harvesting antenna named chlorosome to the RC core where charge separation occurs. In vivo, one RC was found to bind two FMOs, however, the intact structure of RCC as well as the energy transfer mechanism within RCC remain to be clarified. Here we report a structure of intact RCC which contains a RC core and two FMO trimers from a thermophilic green sulfur bacterium Chlorobaculum tepidum at 2.9 Å resolution by cryo‐electron microscopy. The second FMO trimer is attached at the cytoplasmic side asymmetrically relative to the first FMO trimer reported previously. We also observed two new subunits (PscE and PscF) and the N‐terminal transmembrane domain of a cytochrome‐containing subunit (PscC) in the structure. These two novel subunits possibly function to facilitate the binding of FMOs to RC core and to stabilize the whole complex. A new bacteriochlorophyll (numbered as 816) was identified at the interspace between PscF and PscA‐1, causing an asymmetrical energy transfer from the two FMO trimers to RC core. Based on the structure, we propose an energy transfer network within this photosynthetic apparatus. The structure of the intact photosynthetic complex of the green sulfur bacterium Chlorobaculum tepidum contains one reaction center, two asymmetrically binding Fenna‐Matthews‐Olson protein trimers, two novel subunits, and a new bacteriochlorophyll, providing insight into the energy transfer network within this photosynthetic apparatus.</abstract><cop>China (Republic : 1949- )</cop><pub>Wiley Subscription Services, Inc</pub><pmid>36125941</pmid><doi>10.1111/jipb.13367</doi><tpages>12</tpages></addata></record>
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subjects Antennas
Asymmetry
Bacteria
Bacterial Proteins - metabolism
Bacteriochlorophyll
Carcinoma, Renal Cell
Chlorobi - chemistry
Chlorobi - metabolism
Cryoelectron Microscopy
cryo‐electron microscopy
Cytochrome
Cytochromes
Electron microscopy
Energy transfer
FMO protein
Green sulfur bacteria
green sulfur bacterium
Kidney Neoplasms
Microscopy
Photosynthesis
Photosynthetic apparatus
Photosynthetic Reaction Center Complex Proteins - chemistry
Photosynthetic Reaction Center Complex Proteins - metabolism
reaction center
Sulfur
Sulfur bacteria
Trimers
title Cryo‐electron microscopy structure of the intact photosynthetic light‐harvesting antenna‐reaction center complex from a green sulfur bacterium
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